Specialized androgen synthesis in skeletal muscles that actuate elaborate social displays.

Abstract

Androgens mediate the expression of many reproductive behaviors, including the elaborate displays used to navigate courtship and territorial interactions. In some vertebrates, males can produce androgen-dependent sexual behavior even when levels of testosterone (T) is low in the bloodstream. One idea is that select tissues make their own androgens from scratch to support behavioral performance. We first study this phenomenon in the skeletal muscles that actuate elaborate sociosexual displays in downy woodpeckers and two songbirds. We show that the woodpecker display muscle maintains elevated T when the testes are regressed in the non-breeding season. Both the display muscles of woodpeckers, as well as the display muscles in the avian vocal organ (syrinx or SYR) of songbirds, express all transporters and enzymes necessary to convert cholesterol into bioactive androgens locally. In a final analysis, we broaden our study by looking for these same transporters and enzymes in mammalian muscles that operate at different speeds. Using RNA-seq data, we find that the capacity for de novo synthesis is only present in "superfast" extraocular muscle. Together, our results suggest that skeletal muscle specialized to generate extraordinary twitch-times and/or extremely rapid contractile speeds may depend on androgenic hormones produced locally within the muscle itself. Our study therefore uncovers an important new dimension of androgenic regulation of behavior.